Placental homogeneity: Characterizing transcriptional variation among equine chorioallantoic locations.
Abstract: The proper function of the placenta is essential for the health and growth of the fetus and the mother. The placenta relies on dynamic gene expression for its correct and timely development and function. Although numerous studies have identified genes vital for placental functions, equine placental molecular research has primarily focused on single placental locations, in sharp contrast with the broader approach in human studies. Here, we hypothesized that the molecular differences across different regions of the equine placenta are negligible because of its diffuse placental type with a macroscopic homogenous distribution of villi across the placental surface. We compared the transcriptome and stereological findings of the body, pregnant horn, and non-pregnant horn within the equine chorioallantois. Our transcriptomic analysis indicates that the variation between regions of the placenta within individuals is less than the variation observed between individuals. A low number of differentially expressed genes (DEGs) (n = 8) was identified when comparing pregnant and non-pregnant horns within the same placenta, suggesting a remarkable molecular uniformity. A higher number of DEGs was identified when comparing each horn to the body (193 DEGs comparing pregnant horn with body and 207 DEGs comparing non-pregnant horn with body). Genes with a higher expression in the body were associated with processes such as extracellular matrix synthesis and remodeling, which is relevant for placental maturation and placenta-endometrial separation at term and implies asynchrony of these processes across locations. The stereological analysis showed no differences in microcotyledonary density, and width between the locations. However, we observed a greater chorioallantoic thickness in the body and pregnant horn compared to the non-pregnant horn. Overall, our findings reveal a uniform transcriptomic profile across the placental horns, alongside a more distinct gene expression pattern between the uterine body and horns. These regional differences in gene expression suggest a different pace in the placental maturation and detachment among the placental locations.
Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved.
Publication Date: 2024-08-14 PubMed ID: 39167835DOI: 10.1016/j.theriogenology.2024.08.019Google Scholar: Lookup
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- Journal Article
Summary
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Overview
- This research investigates the variation in gene expression across different regions of the horse placenta, concluding that while most placental regions show uniform molecular profiles, there are notable differences between the uterine body and the horns, indicating regional differences in placental maturation and function.
Introduction and Research Motivation
- The placenta is vital for the health and development of both fetus and mother, relying on dynamic gene expression to function properly.
- Previous equine placental studies have often focused on single locations of the placenta, unlike human studies that examine multiple placental regions for comprehensive understanding.
- The equine placenta is classified as a diffuse placenta with an apparently uniform distribution of villi over its surface, leading to the hypothesis that molecular differences across its regions are minimal.
Research Objectives
- To characterize transcriptional variations between different anatomical regions of the equine chorioallantoic placenta: the uterine body, pregnant horn, and non-pregnant horn.
- To assess if gene expression differences in these regions are significant or negligible, thereby confirming or challenging the hypothesis of molecular uniformity.
Methodology
- Sample Collection: Placental tissues were collected from the body, pregnant horn, and non-pregnant horn within individual horse placentas.
- Transcriptomic Analysis: Global gene expression profiling (transcriptome analysis) was performed to identify differentially expressed genes (DEGs) between regions.
- Stereological Analysis: Quantitative microscopic analysis was used to measure tissue features such as microcotyledonary density, width, and chorioallantoic thickness across regions.
Key Findings – Transcriptomic Analysis
- Variation in gene expression between different placental regions within the same individual was mostly less than the variation observed between different individuals, showing individual variability exceeds regional differences.
- When comparing pregnant and non-pregnant horns, only 8 genes were differentially expressed, indicating strong molecular uniformity between these two horns.
- Comparison of each horn (pregnant and non-pregnant) with the uterine body revealed many more DEGs (193 and 207 genes respectively), showing a distinct gene expression pattern between horns and the body.
- Genes more highly expressed in the uterine body were mainly involved in extracellular matrix synthesis and remodeling, processes important for placental maturation and the separation of placenta from the endometrium at birth.
- These gene expression differences imply that placental maturation at the body is occurring asynchronously (at a different pace) compared to the horns.
Key Findings – Stereological Analysis
- Microcotyledonary density and width were similar between all placental locations, suggesting anatomical microstructure is largely uniform across placental regions.
- The chorioallantoic membrane was thicker in the uterine body and pregnant horn than in the non-pregnant horn, indicating some regional morphological differences.
Conclusions and Implications
- The horse placenta exhibits strong transcriptomic homogeneity across the two uterine horns, validating the idea of regional molecular uniformity within these areas.
- However, the uterine body shows distinct gene expression patterns indicating it undergoes differing functional processes such as extracellular matrix remodeling at a different rate or phase.
- These regional differences in gene expression and morphology may reflect differences in placental maturation timing and the detachment process during parturition.
- The findings contribute to equine reproductive biology by highlighting that despite the macroscopic homogeneity of the equine placenta, subtle molecular and structural differences exist with potential functional importance.
- Future equine placental studies should consider sampling site as it may affect gene expression related to placental function and maturity.
Cite This Article
APA
Verstraete MH, Dini P, Orellana D, Uribe-Salazar JM, Veras MM, Carneiro F, Daels P, Fernandes CB.
(2024).
Placental homogeneity: Characterizing transcriptional variation among equine chorioallantoic locations.
Theriogenology, 229, 75-82.
https://doi.org/10.1016/j.theriogenology.2024.08.019 Publication
Researcher Affiliations
- Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA, USA; Department of Morphology, Imaging, Orthopedics, Rehabilitation and Nutrition, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
- Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA, USA. Electronic address: pdini@ucdavis.edu.
- Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA, USA.
- Genome Center, University of California Davis, California, USA.
- Laboratory of environmental and experimental pathology, School of medicine, University of São Paulo, Brazil.
- Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Brazil.
- Department of Morphology, Imaging, Orthopedics, Rehabilitation and Nutrition, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
- Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Brazil.
MeSH Terms
- Female
- Animals
- Horses / genetics
- Horses / physiology
- Pregnancy
- Placenta / metabolism
- Transcriptome
- Chorioallantoic Membrane / metabolism
- Gene Expression Profiling
- Gene Expression Regulation / physiology
Conflict of Interest Statement
Declaration of competing interest The authors have no conflicts of interest to declare.
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